The bitter barricading of prostaglandin biosynthesis pathway: understanding the molecular mechanism of selective cyclooxygenase-2 inhibition by amarogentin, a secoiridoid glycoside from Swertia chirayita

PLoS One. 2014 Mar 6;9(6):e90637. doi: 10.1371/journal.pone.0090637. eCollection 2014.

Abstract

Swertia chirayita, a medicinal herb inhabiting the challenging terrains and high altitudes of the Himalayas, is a rich source of essential phytochemical isolates. Amarogentin, a bitter secoiridoid glycoside from S. chirayita, shows varied activity in several patho-physiological conditions, predominantly in leishmaniasis and carcinogenesis. Experimental analysis has revealed that amarogentin downregulates the cyclooxygenase-2 (COX-2) activity and helps to curtail skin carcinogenesis in mouse models; however, there exists no account on selective inhibition of the inducible cyclooxygenase (COX) isoform by amarogentin. Hence the computer-aided drug discovery methods were used to unravel the COX-2 inhibitory mechanism of amarogentin and to check its selectivity for the inducible isoform over the constitutive one. The generated theoretical models of both isoforms were subjected to molecular docking analysis with amarogentin and twenty-one other Food and Drug Authority (FDA) approved lead molecules. The post-docking binding energy profile of amarogentin was comparable to the binding energy profiles of the FDA approved selective COX-2 inhibitors. Subsequent molecular dynamics simulation analysis delineated the difference in the stability of both complexes, with amarogentin-COX-2 complex being more stable after 40ns simulation. The total binding free energy calculated by MMGBSA for the amarogentin-COX-2 complex was -52.35 KCal/mol against a binding free energy of -8.57 KCal/mol for amarogentin-COX-1 complex, suggesting a possible selective inhibition of the COX-2 protein by the natural inhibitor. Amarogentin achieves this potential selectivity by small, yet significant, structural differences inherent to the binding cavities of the two isoforms. Hypothetically, it might block the entry of the natural substrates in the hydrophobic binding channel of the COX-2, inhibiting the cyclooxygenation step. To sum up briefly, this work highlights the mechanism of the possible selective COX-2 inhibition by amarogentin and endorses the possibility of obtaining efficient, futuristic and targeted therapeutic agents for relieving inflammation and malignancy from this phytochemical source.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acid Motifs
  • Biosynthetic Pathways / drug effects
  • Catalytic Domain
  • Cyclooxygenase 1 / chemistry*
  • Cyclooxygenase 2 / chemistry*
  • Cyclooxygenase 2 Inhibitors / chemistry*
  • Enzyme Stability
  • Humans
  • Hydrogen Bonding
  • Hydrophobic and Hydrophilic Interactions
  • Iridoids / chemistry*
  • Molecular Docking Simulation
  • Molecular Dynamics Simulation
  • Prostaglandins / biosynthesis*
  • Protein Binding
  • Structural Homology, Protein
  • Swertia / chemistry
  • Thermodynamics

Substances

  • Cyclooxygenase 2 Inhibitors
  • Iridoids
  • Prostaglandins
  • amarogentin
  • Cyclooxygenase 1
  • Cyclooxygenase 2
  • PTGS1 protein, human
  • PTGS2 protein, human

Grants and funding

The project was funded by the Department of Biotechnology, Government of India grant to Sub-Distributed Information Centre, IBSD, Imphal, SAN No. 102/IFD/SAN/3287/2005-2006. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.